Poppy Watson

Corticostriatal Connectivity Underlies Individual Differences in the Balance between Habitual and Goal-Directed Action Control

Why are some individuals more susceptible to the formation of inflexible habits than others? In the present study, we used diffusion tensor imaging to demonstrate that brain connectivity predicts individual differences in relative goal-directed and habitual behavioral control in humans. Specifically, vulnerability to habitual “slips of action” toward no-longer-rewarding outcomes was predicted by estimated white matter tract strength in the premotor cortex seeded from the posterior putamen (as well as by gray matter density in the posterior putamen as determined with voxel-based morphometry). In contrast, flexible goal-directed action was predicted by estimated tract strength in the ventromedial prefrontal cortex seeded from the caudate. These findings suggest that integrity of dissociable corticostriatal pathways underlies individual differences in action control in the healthy population, which may ultimately mediate vulnerability to impulse control disorders.

Working for food you don't desire. Cues interfere with goal-directed food-seeking

Why do we indulge in food-seeking and eating behaviors at times when we are already fully sated? In the present study we investigated the hypothesis that food-associated cues in the environment can interfere with goal-directed action by eliciting food-seeking that is independent of the current desirability of the outcome. To this end, we used a computerized task in which participants learned to press keys for chocolate and popcorn rewards. Subsequently, we investigated whether satiation on one of these rewards would bias choice toward the other, still desirable, food reward. We found that satiation did indeed selectively reduce responding on the associated key in the absence of food-associated cues. In contrast, in a Pavlovian-instrumental transfer (PIT) test, satiation failed to reduce cue-elicited food-seeking: in line with our hypothesis, cues that had previously been paired with chocolate and popcorn led to increased responding for the signaled food reward, independent of satiation. Furthermore, we show that food-associated cues will not only bias choice toward the signaled food (outcome-specific transfer), but also enhance the vigor of responding generally (general transfer). These findings point to a mechanism that may underlie the powerful control that cues in our obesogenic environment exert over our behavior.

Cannabis dependence, cognitive control and attentional bias for cannabis words

One of the characteristics of people suffering from addictive behaviors is the tendency to be distracted by drug cues. This attentional bias for drug cues is thought to lead to increased craving and drug use, and may draw individuals into a vicious cycle of drug addiction. In the current study we developed a Dutch version of the cannabis Stroop task and measured attentional bias for cannabis words in a group of heavy cannabis users and matched controls. The classical Stroop task was used as a global measure of cognitive control and we examined the relationship between cognitive control, cannabis-related problems, cannabis craving and cannabis attentional bias. Using our version of the cannabis Stroop task, a group of heavy cannabis users showed attentional bias to cannabis words, whereas a control group of non-users did not. Furthermore, within the group of cannabis users, those who were clinically recognized as dependent showed a stronger attentional bias than the heavy, non-dependent users. Cannabis users who displayed reduced cognitive control (as measured with the classical Stroop task) showed increased session-induced craving. Contrary to expectations, however, cognitive control did not appear to modulate the relationship between attentional bias to cannabis words (cannabis Stroop task) and cannabis dependence. This study confirmed the relationship between cannabis dependence and attentional bias and extends this by highlighting a moderating role for cognitive control, which may make some more vulnerable to craving.

Motivational mechanisms and outcome expectancies underlying the approach bias toward addictive substances

Human behavior can be paradoxical, in that actions can be initiated that are seemingly incongruent with an individual’s explicit desires. This is most commonly observed in drug addiction, where maladaptive behavior (i.e., drug seeking) appears to be compulsive, continuing at great personal cost. Approach biases toward addictive substances have been correlated with actual drug-use in a number of studies, suggesting that this measure can, in some cases, index everyday maladaptive tendencies. At present it is unclear whether this bias to drug cues is a Pavlovian conditioned approach response, a habitual response, the result of a Pavlovian-instrumental transfer process, or a goal-directed action in the sense that expectancy of the rewarding effects of drugs controls approach. We consider this question by combining the theoretical framework of associative learning with the available evidence from approach bias research. Although research investigating the relative contributions of these mechanisms to the approach bias is to date relatively limited, we review existing studies and also outline avenues for future research.

Motivational mechanisms underlying the approach bias to cigarettes

Approach Avoidance tasks measure approach bias, a behavioral tendency to be faster at approaching rather than avoiding drug cues. Approach bias has been measured in a number of different drug-using populations and there is evidence to suggest that approach bias measurements correlate with drug use. Little is known, however, about the motivational mechanisms underlying the approach bias. In the current study we assessed whether the approach bias to cigarettes was immediately sensitive to changes in the incentive value of smoking. We examined the change from baseline in a participant group, after half the group had been given the opportunity to smoke. Specifically, we examined whether the approach bias has the characteristics of a cue-elicited behavior or is flexibly modulated by current desire. Results showed that while the baseline approach-bias score in deprived cigarette smokers correlated with craving, smoking a cigarette led to reduced craving but an increased approach bias score. We discuss a possible account of these findings in terms of an ideomotor outcome-response priming mechanism.

Individual differences in risky decision-making among seniors reflect increased reward sensitivity

Increasing age is associated with subtle but meaningful changes in decision-making. It is unknown, however, to what degree these psychological changes are reflective of age-related changes in decision quality. Here, we investigated the effect of age on latent cognitive processes associated with risky decision-making on the Balloon Analog Risk Task (BART). In the BART, participants repetitively inflate a balloon in order to increase potential reward. At any point, participants can decide to cash-out to harvest the reward, or they can continue, risking a balloon pop that erases all earnings. We found that among seniors, increasing age was associated with greater reward-related risk taking when the balloon has a higher probability of popping (i.e., a “high risk” condition). Cognitive modeling results from hierarchical Bayesian estimation suggested that performance differences were due to increased reward sensitivity in high risk conditions in seniors.

Dissociable corticostriatal circuits underlie goal-directed vs. cue-elicited habitual food seeking after satiation: evidence from a multimodal MRI study

The present multimodal MRI study advances our understanding of the corticostriatal circuits underlying goal‐directed vs. cue‐driven, habitual food seeking. To this end, we employed a computerized Pavlovian‐instrumental transfer paradigm. During the test phase, participants were free to perform learned instrumental responses (left and right key presses) for popcorn and Smarties outcomes. Importantly, prior to this test half of the participants had been sated on popcorn and the other half on Smarties – resulting in a reduced desirability of those outcomes. Furthermore, during a proportion of the test trials, food‐associated Pavlovian cues were presented in the background. In line with previous studies, we found that participants were able to perform in a goal‐directed manner in the absence of Pavlovian cues, meaning that specific satiation selectively reduced responding for that food. However, presentation of Pavlovian cues biased choice toward the associated food reward regardless of satiation. Functional MRI analyses revealed that, in the absence of Pavlovian cues, posterior ventromedial prefrontal cortex tracked outcome value. In contrast, during cued trials, the BOLD signal in the posterior putamen differentiated between responses compatible and incompatible with the cue‐associated outcome. Furthermore, we identified a region in ventral amygdala showing relatively strong functional connectivity with posterior putamen during the cued trials. Structural MRI analyses provided converging evidence for the involvement of corticostriatal circuits: diffusion tensor imaging data revealed that connectivity of caudate‐seeded white‐matter tracts to the ventromedial prefrontal cortex predicted responding for still‐valuable outcomes; and gray matter integrity in the premotor cortex predicted individual Pavlovian cueing effects.

Stimulus Control Over Action for Food in Obese versus Healthy-weight Individuals

In the current study we examined an associative learning mechanism by which food cues (signaling low- versus high-calorie food) can bias instrumental responses directed toward those foods. To investigate the clinical relevance of this mechanism, we used a computerized Pavlovian-to-instrumental transfer task and compared performance of 19 severely obese individuals to that of 19 healthy-weight controls matched for age, education and gender. During the response-priming test we exposed participants to both food pictures and to Pavlovian cues predictive of those food pictures, and examined their biasing effect on instrumental choice. As expected, obese participants showed higher priming rates for palatable, high-calorie foods (potato chips and chocolate) relative to low-calorie foods (lettuce and courgette) whereas healthy-weight individuals did not show a difference between priming rates for these two food types. We also included various measures of impulsivity as well as a slips-of-action task designed to investigate the balance between goal-directed and habitual behavioral control in these two groups. We did not find any evidence of increased impulsivity or reliance on a habitual strategy during the slips-of-action task, in obese participants. General Scientific Summary: Our environment is full of cues signaling the availability of tasty, but often unhealthy, foods. This study suggests that severely obese individuals are particularly sensitive to high-calorie food cues whereas low-calorie food cues have little effect on their behavior.

Current limits of experimental research into habits and future directions

The outcome devaluation paradigm allows for the differentiation between goal-directed actions and habits and has been used extensively in both animal and human studies. This has been a fruitful avenue of research with translational human research reporting reduced sensitivity to devaluation in a number of clinical populations using various different paradigms. However, these paradigms do not provide a direct window on the extent to which impaired performance is due to strong habit formation or to weak goal-directed control. We review the indirect nature of the existing evidence from both animal and human studies and suggest avenues for future research including combining behavioral repetition with manipulations to reduce goal-directed control processes as well as alternative paradigms such as the Pavlovian-to-instrumental transfer task.

Limits of ideomotor action–outcome acquisition

Ideomotor theory proposes that goal-directed action emerges from the implicit, incidental acquisition of bi-directional associations between actions and their outcomes. In line with this idea, a simple two-stage priming paradigm has provided evidence that presentation of outcomes primes previously associated actions. In the current study we compare the standard priming paradigm with two actions and two unique outcomes (Experiment 1) with two more complex, but otherwise identical versions (Experiment 2: two vs. four actions with four outcomes). Our results show stronger evidence of action-outcome learning in the simple compared to the more complex versions. We suggest that, when using the classic two-stage paradigm, action-outcome acquisition is limited to just a few action-outcome associations that can be concurrently learned-at least if learning is not supported by discriminative stimuli and outcomes are not salient or motivationally relevant. This article is part of a Special Issue entitled SI: Prediction and Attention.